Periodontal Comparison on Systemic Lupus Erythematosus Patients and Healthy Subjects: A Cross-Sectional Study

Nanda Rachmad Putra  Gofur; Kusworini  Handono; Nurdiana  Nurdiana; Handono  Kalim

Authors

Nanda Rachmad Putra Gofur
Kusworini Handono
Nurdiana Nurdiana
Handono Kalim

Keywords:

Connective Tissue Diseases, Oral Health, Periodontics, Periodontal Index

Abstract

Objective: To analyze periodontal comparison between Systemic Lupus Erythematosus (SLE) subject and healthy control. Material and Methods: This descriptive cross-sectional study included 122 subjects, 61 SLE patients and 61 healthy subjects who visited the Rheumatology Department, Dr. Saiful Anwar General Hospital, Malang, during 2017-2018. Clinical examination of SLE was using Mexican SLE Disease Activity Index and oral cavity conditions were assessed using the periodontal index, gingival index, calculus index, bleeding on probing, clinical attachment loss and mobility teeth. Results: The age of SLE patients ranged from 18-55 years old with the mean age of 29.50 ± 9.57 years old. Periodontitis was higher in SLE patients (88.5%) than healthy subjects (22.95%). In addition, periodontitis occurrence in SLE (2.66 ± 1.02) was significantly different (p<0.001) compared to healthy subjects (0.51 ± 0.81). Conclusion: This study found higher rates of periodontitis, gingivitis, bleeding on probing, clinical attachment loss, and mobility tooth among SLE patients compared to healthy subjects. Periodontitis was also found to be higher along with more severe SLE group.

References

Fabbri C, Fuller R, Bonfa E, Guedes LK, D’Alleva PS, Borba EF. Periodontitis treatment improves systemic lupus erythematosus response to immunosuppressive therapy. Clin Rheumatol 2014; 33(4):505-9. https://doi.org/10.1007/s10067-013-2473-2

Bartold PM, van Dyke TE. Periodontitis: a host-mediated disruption of microbial homeostasis. Unlearning learned concepts. Periodontol 2000 2013; 62(1):203-17. https://doi.org/10.1111/j.1600-0757.2012.00450.x

Cullinan MP, Seymour GJ. Periodontal disease and systemic illness: Will the evidence ever be enough? Periodontol 2000 2013; 62(1):271-86. https://doi.org/10.1111/prd.12007

Genco RJ, Borgnakke WS. Risk factors for periodontal disease. Periodontol 2000 2013; 62(1):59-94. https://doi.org/10.1111/j.1600-0757.2012.00457.x

Ebersole JL, Dawson DR, Morford LA, Peyyala R, Miller, CS, Gonzaléz OA. Periodontal disease immunology: ‘Double indemnity’ in protecting the host. Periodontol 2000 2013; 62(1):163-202. https://doi.org/10.1111/prd.12005

Calderaro DC, FerreiraGA, Correa JD, Mendonca SM, Silva TA, Costa FO, et al. Is chronic periodontitis premature in systemic lupus erythematosus patients? Clin Rheumatol 2017; 36(3):713-8. https://doi.org/10.1007/s10067-016-3385-8

Rutter-Locher Z, Fuggle N, Orlandi M, D’Aiuto F, Sofat N. Periodontal Disease and Autoimmunity: What We Have Learned From Microbiome in Rheumatology. In: Arjunan P. Periodontitis - A Useful Reference. London: IntechOpen Limited; 2017.

Kobayashi T, Ito S, Yamamoto K, Hasegawa H, Sugita N, Kuroda T, et al. Risk of periodontitis in systemic lupus erythematosus is associated with Fcγ receptor polymorphisms. J Periodontol 2003; 74(3):378-84. https://doi.org/10.1902/jop.2003.74.3.378

Russel AL. The periodontal index. J Periodontol 1967; 38(6P2):585-91. https://doi.org/10.1902/jop.1967.38.6_part2.585

Beltrán-Aguilar ED, Eke PI, Thornton-Evans G, Petersen PE. Recording and surveillance systems for periodontal diseases. Periodontology 2000 2012; 60(1):40-53. https://doi.org/10.1111/j.1600-0757.2012.00446.x

Rebelo MAB, Queiroz AC. Gingival Indices: State of Art. In: Panagakos FS, Davies RM. Gingival Diseases - Their Aetiology, Prevention and Treatment. London: IntechOpen Limited; 2011. pp. 41-54.

Mukaka MM. A guide to appropriate use of correlation coefficient in medical research. Malawi Med J 2012; 24(3):69-71.

Albandar JM, Susin C, Hughes FJ. Manifestations of systemic diseases and conditions that affect the periodontal attachment apparatus: Case definitions and diagnostic considerations. J Periodontol 2018; 89(Suppl1):S183-S203. https://doi.org/10.1002/JPER.16-0480

Rees F, Doherty M, Grainge MJ, Lanyon P, Zhang W. The worldwide incidence and prevalence of systemic lupus erythematosus: a systematic review of epidemiological studies. Rheumatology 2017; 56(11):1945-61. https://doi.org/10.1093/rheumatology/kex260

Wu YD, Lin CH, Chao WC, Liao TL, Chen DY, Chen HH. Association between a history of periodontitis and the risk of systemic lupus erythematosus: A nationwide, population-based, case-control study. PloS One 2017; 12(10):e0187075. https://doi.org/10.1371/journal.pone.0187075

Al-Mutairi KD, Al-Zahrani, MS, Bahlas SM, Kahyal RA, Zawawi KH. Periodontal findings in systemic lupus erythematosus patients and healthy controls. Saudi Med J 2015; 36(4):463-8. https://doi.org/10.15537/smj.2015.4.1074

Hammoudeh M, Al-Momani A, Sarakbi H, Chandra P, Hammoudeh S. Oral manifestations of systemic lupus erythematosus patients in Qatar: a pilot study. Int J Rheumatol 2018; 2018:6052326. https://doi.org/10.1155/2018/6052326

Nair S, Faizuddin M, Dharmapalan J. Role of autoimmune responses in periodontal disease. Autoimmune Dis 2014; 2014:596824. https://doi.org/10.1155/2014/596824

Manjarrez-orduño N, Menard LC, Carman JA, Suchard SJ, Casano F, Lee D, et al. A systemic lupus erythematosus endophenotype characterized by increased CD8 cytotoxic signature associates with renal involvement. ImmunoHorizons 2017; 1(7):124-32.

Kaur G, Mohindra K, Singla S. Autoimmunity: Basics and link with periodontal disease. Autoimmun Rev 2016; 8:71-4.

Fukushima Y, Minato N, Hattori M. The impact of senescence-associated T cells on immunosenescence and age-related disorders. Inflamm Regen 2018; 38:24. https://doi.org/10.1186/s41232-018-0082-9

Shah D, Mahajan N, Sah S, Nath SK, Paudyal B. Oxidative stress and its biomarkers in systemic lupus erythematosus. J Biomed Sci 2014; 21(1):18-23.

Perl A, Hanczko R, Doherty E. Assessment of mitochondrial dysfunction in lymphocytes of patients with systemic lupus erythematosus. Methods Mol Biol 2012; 900:61-89. https://doi.org/10.1007/978-1-60761-720-4_4

Gofur NRP, Handono K, Nurdiana N, Kalim H. Association of Th–Tc protein CD28+ and periodontal inflammation among Indonesian women with SLE disease. Sys Rev Pharm 2020; 11(6):580-6.

Gofur NRP. Impact of SARS-CoV-2 on periodontal tissue manifestation. J Int Oral Health 2020; 12(8):S90-S92.

Handono K, Gofur NRP, Nurdiana, Kalim H, Wahono CS, Poeranto S. Gingivitis on Systemic Lupus Erythematosus (SLE) patients: a pilot study. Res J Pharm Tech 2020; 13(11):5466-70. https://doi.org/10.5958/0974-360X.2020.00954.3

Gofur NRP, Handono K, Nurdiana N, Kalim H. Periodontitis is associated with disease severity and anti-double stranded DNA antibody and interferon-gamma levels in patients with systemic lupus erythematosus. J Taibah Univ Med Sci 2019; 14(6):560-5. https://doi.org/10.1016/j.jtumed.2019.09.005

Gofur NRP, Nurdiana N, Handono K, Kalim H. Periodontal tissue condition on systemic lupus erythematosus patients: a clinical study. Pesqui Bras Odontopediatria Clín Integr 2020; 20(1):e5094. https://doi.org/10.1590/pboci.2020.010

Gofur NRP, Nurdiana N, Handono K, Kalim H. Immune aging marker associated with periodontitis in systemic lupus erythematosus patients. AIP Conf Proc 2019; 5(1)1-11. https://doi.org/10.1063/1.5109978

Handono K, Gofur NRP, Nurdiana N, Kalim H, Wahono CS, Poeranto S, et al. Role of lymphocytes CD4/CD8 ratio and immunoglobulin G cytomegalovirus as potential markers for systemic lupus erythematosus patients with periodontal disease. Eur J Dent 2020; 14(4):544-50. https://doi.org/10.1055/s-0040-1715788